Genomic diversity and functional potential of facultative bacterial symbionts across scale insects

Abstract

Microbial symbionts play pivotal roles in the physiology, ecology, and evolution of insects. While obligate symbionts have been extensively characterized in insects feeding on nutritionally poor diets, the diversity and functional roles of facultative bacterial symbionts remain largely unexplored in many insect lineages, including scale insects (Hemiptera: Coccomorpha). Here, we present a genome-resolved metagenomic and comparative genomic analysis of facultative bacterial symbionts across 120 scale insect metagenomes from 20 different families. Our analyses reveal rich and taxonomically diverse facultative symbiont communities, dominated by the Pseudomonadota, such as Wolbachia, Rickettsia, Arsenophonus, and Sodalis. Genomic features reveal substantial variation in genome sizes, coding densities, metabolic potentials, and hostinteraction genes among symbiont clades, indicating lineage-specific lifestyles and host interactions. Interestingly, alphaproteobacterial and gammaproteobacterial symbionts mostly co-occur within their respective hosts. Gammaproteobacterial symbionts exhibit broader metabolic repertoires and potential defense capabilities via the APSE phage toxin cassettes, while alphaproteobacterial symbionts retain reduced metabolic capabilities, Type IV secretion systems, and reproductive manipulation genes (cifAB and wmk). We propose how the symbiont genes related to nutritional provisioning, defensive symbiosis, and reproductive manipulation may influence the biology and evolution of scale insects. Our results provide the first comprehensive genomic overview of facultative bacterial symbionts in scale insects, revealing their evolutionary dynamics and putative functions.